Evaluating Long-Term Oncologic Outcomes of Radiofrequency Ablation for T1a Renal Cell Carcinoma with Minimum 10 Years of Follow-Up

Abstract

Introduction:

We aimed to assess long-term outcomes of radiofrequency ablation (RFA) for biopsy-proven renal cell carcinoma (RCC), with a minimum follow-up of 10 years.

Methods:

We retrospectively identified patients who underwent RFA for renal masses at our center between 2004 and 2014. All patients who underwent RFA for a single, unilateral renal mass measuring ≤4 cm and had a minimum follow-up of 10 years were included. Our primary outcome was RCC recurrence. Kaplan–Meier curves were used to identify recurrence-free, metastasis-free, cancer-specific, and overall survival rates. Multivariate binary logistic regression was used to determine predictors of recurrence.

Results:

A total of 75 patients were included in our study. Median follow-up was 131 months (interquartile range [IQR], 109–151 months). Median tumor size was 2.7 cm (IQR, 2.1–3.3 cm), and the median RENAL nephrometry score was 7 (IQR, 5–8). A total of 70.7% of pathology results showed clear cell RCC. Nine patients experienced RCC recurrence with a median time to recurrence of 54.4 months (IQR, 17.3–70.3 months). Two patients died due to metastatic RCC, and median time to death was 97.5 months (IQR, 55.8–128 months). Overall recurrence-free survival was 88%, and cancer-specific survival was 97%. No patients developed recurrence after 10 years. Univariate and multivariate regression did not identify any predictors of recurrence.

Conclusion:

RFA is a safe and effective treatment option for T1a RCC. Rates of recurrence and cancer-specific mortality are low at 10 years postprocedure. No patient or tumor factors were identified as predictors for RCC recurrence.

Introduction

Renal cell carcinoma (RCC) is the sixth most frequently diagnosed cancer and the third most commonly diagnosed urologic malignancy worldwide.¹ Increasing utilization of abdominal imaging has led to more frequent identification of incidental small renal masses (SRMs), ultimately resulting in the increasing incidence of RCC.^2,3 Although the gold standard for definitive management of SRMs remains nephron-sparing surgical resection, radiofrequency ablation (RFA) has emerged as a viable minimally invasive treatment modality.

Multiple guidelines recommend RFA as a reasonable alternative to surgery for tumors <3 cm in size.^4,5 Prior studies have suggested that RFA demonstrates similar oncologic outcomes when compared with surgical extirpation, although no prospective randomized controlled trials comparing the two treatment modalities have been published. Thus, these recommendations stem from observational and retrospective studies.⁶ In addition, previous studies that have examined post-RFA outcomes have had a relatively short follow-up period of less than a decade, limiting recommendations for long-term follow-up surveillance.⁷ In this study, we aimed to assess long-term outcomes of RFA for SRMs at a single center with a minimum follow-up of 10 years.

Materials and Methods

Following approval from our institutional research ethics board (HIREB 16763), clinical data were retrospectively queried for patients who underwent RFA for a renal tumor of any size at our academic tertiary medical center between 2004 and 2014. The year 2004 represents the earliest data that had readily accessible images available for extraction, whereas a cutoff date of 2014 allowed for a minimum of 10-year follow-up data.

Inclusion criteria

Patients were included if they had: (1) radiographical evidence of a pT1a (≤4 cm) solitary unilateral solid renal tumor diagnosed on CT or MRI, (2) localized disease, (3) biopsy-proven malignant pathology, and (4) underwent RFA via percutaneous or laparoscopic approach. Patients with familial syndromes with a predisposition to multiple RCCs, biopsy-proven oncocytoma or angiomyolipoma, missing or incomplete biopsies, or previous treatment of RCC on the ipsilateral kidney were excluded.

Procedural details

Eligibility for CT-guided RFA was determined by local interventional radiologists and required the following: (1) an appropriate access trajectory; (2) freedom from neighboring bowel, liver parenchyma, or lung; (3) adequate distance from adjacent structures to avoid collateral heat dissipation; and (4) absence of underlying uncorrectable coagulopathy. The procedure was done under conscious sedation and local anesthesia. The patient was positioned according to the location of the tumor; for posterior tumors, the patient was placed in the prone position, whereas for anterior tumors, the patient was placed in a lateral decubitus position. Following this, under CT guidance, an RFA probe (Cool-tip RFA probe, Medtronic, Sunnyvale, CA) was inserted percutaneously. The ablation zone ranged from 2 to 3 cm in diameter, and the target temperature was 105°C. Throughout the procedure, intravenous (IV) contrast was used to enhance the visualization of the renal tumor under CT imaging.

Eligibility for laparoscopy-guided RFA was determined by the managing urologist based on tumor location, with the most favored tumors being located anteriorly. Laparoscopic RFA was conducted in a similar manner to CT-guided RFA. Probes were inserted percutaneously under laparoscopic guidance after exposure of the renal tumor. Laparoscopic ultrasound was used to confirm proper probe deployment. The probe tines were deployed 5–10 mm beyond the diameter of the lesion, and ablation was performed to a target temperature of 105°C.

Data collection

Study data were collected and managed using REDCap (Research Electronic Data Capture) electronic data capture tool, hosted at St. Joseph’s Hospital.^8,9 Data extraction included baseline demographics, treatment details, perioperative complications, tumor characteristics (grade, size, pathology, laterality), nephrometry score, change in estimated glomerular filtration rate (eGFR), and RCC recurrence. The RENAL nephrometry score was determined based on contrast-enhanced CT cross-sectional imaging by two authors after independent assessment and agreement (M.U. and M.A.).^10
–12 Complications were categorized by Clavien–Dindo classification; grade I-II complications were classified as minor complications and grade III-V complications were classified as major complications.

Effective ablation was defined as no residual mass or a nonenhancing (increase of ≤ 10 HUs compared with precontrast imaging) mass following RFA on a postprocedural CT with IV contrast. Follow-up after RFA was scheduled as per the Canadian Urological Association (CUA) guidelines.⁷ All tumor recurrences were confirmed using conventional CT of the abdomen and pelvis with IV contrast. Recurrence was defined as either (1) local recurrence with measurable enhancement (increase of >10 HUs compared with precontrast imaging) after RFA with respect to new or residual disease at the ipsilateral kidney, (2) distant recurrence with a new lesion presumed to be metastatic RCC in the absence of a formal biopsy, or (3) biopsy-proven metastatic disease. A new lesion was defined as an enhancing lesion found outside of the primary ablation site, or an enhancing lesion at the primary ablation site after diagnostic imaging evidence of prior effective ablation.

Statistical analysis

Descriptive statistics were used to summarize patient demographics. A p-value of <0.05 was considered statistically significant. The normality of continuous variables was tested with the Shapiro–Wilk test; normally distributed data were presented as mean with standard deviation (SD), whereas data within non-normal distributions were presented as a median with interquartile range (IQR). The paired-samples t-test was used to compare pre- and post-RFA eGFR. Kaplan–Meier curves were used to determine recurrence-free survival (RFS), metastasis-free survival (MFS), cancer-specific survival (CSS), and overall survival (OS).

Univariate models and multivariate binary logistic regression were used to determine predictors for recurrence. Covariates were chosen a priori based on prior published data and included age at the time of treatment, biological sex, tumor size, biopsy pathology, approach (percutaneous or laparoscopic), grade, and RENAL nephrometry score.^13,14 Statistical analysis was performed using IBM SPSS Statistics v28.0 (IBM, Armonk, NY).

Results

Patient demographics and tumor characteristics

We identified 75 patients who met our inclusion criteria and underwent RFA for treatment of an SRM between 2004 and 2014 (Table 1). Median follow-up was 131 months (IQR, 109–151 months). Median age at the time of procedure was 68 years (IQR, 61–75 years), and 26.7% of patients were female.

Table 1.

Demographic Data and Tumor Characteristics

Patient characteristics
Patients	75
Median follow-up (months) (IQR)	131 (32)
Female (%)	26.7
Median age at procedure (years) (IQR)	68 (14)
Median tumor size (cm) (IQR)	2.7 (1.2)
Laterality, right (%)	50.7
Solitary kidney (%)	10.7
RENAL score (IQR)	7 (3)
Low (4–6) (%)	49
Medium (7–9) (%)	51
High (10–12) (%)	0
Histology (%)
Clear cell	70.7
Papillary type 1	22.7
Papillary type 2	2.7
Chromophobe	4
Grade (%)
GX	56
G1	20
G2	22.7
G3	1.3
G4	0

IQR = interquartile range.

The median tumor size was 2.7 cm (IQR, 2.1–3.3 cm) and the median RENAL nephrometry score was 7 (IQR, 5–8). In total, 50.7% of tumors were right-sided, and 10.7% of tumors were in a solitary kidney. The majority (70.7%) of pathology results showed clear cell RCC. The majority of tumors (56%) could not have their grade assessed and were therefore classified as GX. Of those tumors that had a recorded grade, most were classified as grade 1 (20%) or grade 2 (23%), with only a single patient showing grade 3 histology.

Nononcologic outcomes

The majority (73.3%) of patients underwent RFA via a percutaneous approach (Table 2). Four patients (5.3%) had incomplete ablation requiring retreatment. When evaluating post-RFA change in renal function, eGFR at 1 year was found to be significantly lower, with a mean difference of 4.2 mL/min/1.73 m² (SD = 10.2 mL/min/1.73 m²) (p = 0.006).

Table 2.

Radiofrequency Ablation Approach and Complications

Number of tumor technical success (%)
Approach (%)
Percutaneous	73.3
Laparoscopic	26.7
Complications (%)
Total	17.3
Major complications	1.3
Transfusion rate (%)	5.3
Incomplete ablation needing re-ablation (%)	5.3

The overall complication rate was 17.3%, with the only major complication being a single case (1.3%) of postprocedural bleeding requiring embolization. The other minor complications included hematuria in five patients, pain in four patients, hematoma in one patient, and acute kidney injury in one patient. Four patients (5.3%) required blood transfusions.

Oncologic outcomes

At a minimum of 10-year follow-up, the RFS rate was 88% and the CSS rate was 97%. Nine patients (12%) experienced recurrences, including seven recurrences in the ipsilateral kidney, one mediastinal metastasis, and one adrenal metastasis (Table 3). Among the ipsilateral recurrences, three were at the ablation site and four were at a location other than the ablation site. Seven of these patients had tumors demonstrating clear cell histology, whereas the remaining two had papillary type 1 RCC. The median time to recurrence (TTR) was 54.4 months (IQR, 17.3–70.3 months). Of those individuals with recurrent disease, four died during follow-up; only two of these deaths (3% of all patients) were attributable to RCC, with both patients having developed metastatic disease. The time to death (TTD) for the two patients who died of metastatic RCC was 52 and 119 months. Median TTD for all patients was 97.5 months (IQR, 55.8–128 months). No patients developed RCC recurrence after 10 years.

Table 3.

Patients with Renal Cell Carcinoma Recurrence

Patient number	Sex	Age at time of treatment (years)	RFA approach	Tumor size (cm)	RENAL score	Pathology	Recurrence location	Time to recurrence (months)	Recurrence management	Status at last follow-up	Time to death (months)
1	Male	68	Percutaneous	2.8	5	Papillary type 1	Ipsilateral kidney (other site)	54.4	Surgery	Alive	NA
2	Female	72	Percutaneous	2.6	7	Clear cell	Adrenal	16.8	Surgery	Death from metastatic RCC	52
3	Male	75	Percutaneous	2.4	5	Papillary type 1	Ipsilateral kidney (other site)	62.2	Surveillance	Death from respiratory cause	115
4	Male	69	Percutaneous	3.4	9	Clear cell	Ipsilateral kidney (other site)	66.7	RFA	Alive	NA
5	Female	62	Percutaneous	3.8	8	Clear cell	Ipsilateral kidney (ablation site)	15.4	Surgery	Alive	NA
6	Female	93	Percutaneous	3.9	9	Clear cell	Ipsilateral kidney (ablation site)	17.9	Surveillance	Death from acute respiratory failure	46
7	Male	78	Laparoscopic	2.01	5	Clear cell	Ipsilateral kidney (other site)	98.2	Surgery	Alive	NA
8	Male	73	Percutaneous	2.5	7	Clear cell	Ipsilateral kidney (ablation site)	73.9	RFA	Alive	NA
9	Male	63	Percutaneous	2.5	4	Clear cell	Mediastinum	50.9	Radiation	Death from metastatic RCC	NA

NA = not applicable; RCC = renal cell carcinoma; RFA = radiofrequency ablation.

Figure 1 depicts Kaplan–Meier curves for RFS, MFS, CSS, and OS. At the 10-year follow-up, RFS was 88%, CSS was 97%, MFS was 97%, and OS was 80%. Univariate and multivariate regression did not identify any predictors of recurrence (Supplementary Table S1).

FIG. 1.

Kaplan–Meier curves depicting oncologic outcomes after radiofrequency ablation. (A) Recurrence-free survival (RFS), (B) metastasis-free survival (MFS), (C) cancer-specific survival (CSS), and (D) overall survival (OS).

Discussion

Data on long-term oncologic outcomes of RFA for T1a renal tumors at 10 years and beyond are lacking. In our cohort, with a median follow-up of 131 months, we identified a recurrence rate of 12% and a median TTR of 54.4 months. In addition, no patients experienced a recurrence after 10 years, and the overall CSS rates at 10 years were 97%. Ultimately, only two patients (3%) died because of RCC progression. Only one patient experienced a major complication, a post-RFA bleed requiring embolization, and the transfusion rate among our cohort was 5%. Based on these findings, RFA is a safe treatment modality for T1a RCC and demonstrates a low recurrence rate, especially beyond 10 years post-RFA.

Previous studies with shorter follow-up have reported 10-year RFS rates of 84%–94.2% and 10-year CSS rates of 86%–97% (Supplementary Table S2).^15

–20 These outcomes are concordant with our findings of a 10-year RFS rate of 88% and CSS rate of 97% after RFA for pT1a RCC. Notably, all identified prior studies had a significantly shorter median follow-up compared with our study, ranging from 44.4 to 89 months. To our knowledge, our study is the first to include only patients with at least 10 years of follow-up, which ultimately informs the paucity of data on long-term recurrence after a decade of postprocedural surveillance.

Most guidelines recommend RFA as an alternative treatment modality to partial nephrectomy for patients who wish to avoid or are poor candidates for surgery.^4,5 Minor complications of RFA, such as hematuria, perirenal hematoma, and prolonged pain, can typically be managed conservatively. Major complications, although far less common, can result in significant morbidity and include significant bleeding, tumor seeding to the needle tract, and injury to the collecting system resulting in urine leak or ureteral stricture.^21,22 Prior reports have described complication rates comparable with our overall complication rate of 17.3% and a major complication rate of 1.3%.^23
–25 Additionally, RFA has also demonstrated minimal impact on renal function and can be offered in patients with chronic kidney disease.^26,27 Although our study found that eGFR was significantly decreased by 4.1 ± 10.5 mL/min/1.73 m² at 1 year post-RFA, such a decrease in renal function is unlikely to be clinically significant.

In our study, univariate and multivariate regression identified no association between recurrence and any of the covariates assessed, including age, sex, tumor size, pathology, approach, grade, and RENAL nephrometry score. This is similar to other studies that also did not identify any significant patient or tumor factors that served as predictors of RCC recurrence after RFA for T1a renal tumors.^13,14 Of note, the majority of tumors with an identified grade were grade 1 or 2, indicating that the likelihood of recurrence was likely low in the population. This may have limited our ability to identify any association that may exist between higher grade RCC and recurrence following RFA. Although previous studies have reported that tumor size >4 cm is a predictor for recurrence, this does not apply to our study, in which we only included patients with tumors ≤4 cm in size.^14,28

Our study’s main strength includes its median follow-up of 131 months, which allows for analysis of real-world oncologic outcomes at 10 years post-RFA. However, it is not without its limitations. As a single-center retrospective study, it may be prone to selection bias and its results may not be widely generalizable. However, our results are similar to those reported in prior studies examining 10-year oncologic outcomes after RFA for T1a RCC, suggesting that our results may be generalizable to the larger population. In addition, our study population of 75 is relatively small compared with other similar studies, which may limit our analysis of oncologic outcomes and ability to identify predictors of RCC recurrence. Furthermore, 26.7% of our patients underwent RFA via a laparoscopic approach. Although previous studies have shown no differences in oncologic outcomes and complication rates when comparing laparoscopic with percutaneous RFA, the utilization of different RFA approaches may still have an impact on our results.^24,29,30 Finally, our study contains no control group, preventing direct comparison with other treatment modalities or patient populations.

Conclusion

In summary, we conducted a retrospective single-center study examining oncologic outcomes of RFA for treatment of T1a RCC where we only included patients with a minimum 10-year follow-up. With a median follow-up of 131 months, we identified an RFS rate of 88% and a CSS rate of 97%. The major complication rate was low and both univariate and multivariate regression did not identify any significant predictors of RCC recurrence after RFA. Overall, RFA is a safe and an effective treatment modality for T1a RCC with low rates of recurrence and cancer-specific death at 10 years postprocedure.

Footnotes

Authors’ Contributions

All authors met the criteria for authorship in drafting this article.

Author Disclosure Statement

The authors have no conflicts of interest to declare.

Funding Information

The authors have no financial interests or funding sources to disclose.

Supplementary Material

Supplementary Table S1

Supplementary Table S2

Abbreviations Used

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